Origins of aposematism in poison frogs

Over the last 50 million years, poison frogs (family Dendrobatidae) have evolved to sequester alkaloids from diminutive arthropod prey three independent times. Along with origins of chemical defense, these dendrobatids have undergone extensive changes in metabolism, skin morphology, diet, coloration, behavior, and neurophysiology. Thus, poison frogs present an excellent system for identifying mechanisms underlying the origins and diversification of complex novel phenotypes.

Why don't poison frogs poison themselves? Their chemical defenses target a variety of ion channel proteins in nervous systems that govern action potentials and neurotransmitter release. Any organism susceptible to these chemicals would not survive being covered in them. We study evolutionary changes in nervous system proteins that are targeted by poison frog chemical defenses, such as voltage-gated sodium channels and nicotinic acetylcholine receptors.

Among the 300 species of dendrobatid poison frogs, the Epipedobates clade is the youngest group that is both chemically defended and brightly colored, offering a glimpse into incipient origins of aposematism. By studying the extensive phenotypic variation in Epipedobates, we are illuminating the evolutionary pathways, population dynamics, and molecular mechanisms underlying the complex ecological shift to aposematism.

Evolving toxic flies

Evolutionary transitions underlying large-scale phenotypic change are difficult to study because they often occur over millions of years. However, the fruit fly has a short generation time and a small genome that is well annotated and cheap to sequence. We are using experimental evolution to evolve toxin-sequestering fruit flies. Evolutionary changes in the fruit fly genome, transcriptome, and physiology will generate a model of how chemical defense arises that will inform future studies in poison frogs and other organisms.

A taste for danger

The evolution of acquired neurotoxic defenses requires myriad changes in an organism's nervous system and physiology. The organism must selectively take up chemicals, circumvent detoxification pathways, evolve resistance, and ultimately transport and store chemicals. Interestingly, in frogs, acquired chemical defenses have co-evolved with diurnality and bright coloration, suggesting that chemical defenses allows certain organisms to risk being more visible to predators and perhaps allows them to occupy a new ecological niche. Using target-bait capture, we are sequencing genes involved in these sensory and physiological processes in three clades of aposematic frogs. Behavioral experiments paired with physiological assays will evaluate how identified genetic changes produce novel phenotypes. We are currently broadening these efforts to include toxin-eating snakes from California and Ecuador.

Collections-based research

Large and dynamic gene families are challenging to study in non-model organisms. If these genes could be studied using museum collections, their role in phenotypic diversification could be easily tested across a broad phylogenetic array of organisms. We are collaborating to develop a new method that would reliably quantify gene expression from formalin-fixed museum specimens. If successful, this method will substantially expand the possibilities of collections-based research.